Environmental Oxygen Exposure Allows for the Evolution of Interdigital Cell Death in Limb Patterning

Author: Cordeiro, Ingrid Rosenburg; Kabashima, Kaori; Ochi, Haruki; Munakata, Keijiro; Nishimori, Chika; Laslo, Mara; Hanken, James; Tanaka, Mikiko

Description: Amphibians form fingers without webbing by differential growth between digital and interdigital regions. Amniotes, however, employ interdigital cell death (ICD), an additional mechanism that contributes to a greater variation of limb shapes. Here, we investigate the role of environmental oxygen in the evolution of ICD in tetrapods. While cell death is restricted to the limb margin in amphibians with aquatic tadpoles, Eleutherodactylus coqui, a frog with terrestrial-direct-developing eggs, has cell death in the interdigital region. Chicken requires sufficient oxygen and reactive oxygen species to induce cell death, with the oxygen tension profile itself being distinct between the limbs of chicken and Xenopus laevis frogs. Notably, increasing blood vessel density in X. laevis limbs, as well as incubating tadpoles under high oxygen levels, induces ICD. We propose that the oxygen available to terrestrial eggs was an ecological feature crucial for the evolution of ICD, made possible by conserved autopod-patterning mechanisms.

Subject headings: Animals; Body Patterning; Bone Morphogenetic Proteins; Cell Death; Chick Embryo; Extremities; Larva; Morphogenesis; Oxygen; Reactive Oxygen Species; Xenopus laevis; Bmp signaling; Blood vessels; Evolution; Interdigital cell death; Limb development

Publication year: 2019

Journal or book title: Developmental Cell

Volume: 50

Issue: 2

Pages: 155-166.e4

Find the full text: https://par.nsf.gov/servlets/purl/10135152

Find more like this one (cited by): https://scholar.google.com/scholar?cites=4258727652121263194&as_sdt=1000005&sciodt=0,16&hl=en

Serial number: 3704

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